Zhao et al. BMC Biology (2021) 19:2 https://doi.org/10.1186/s12915-020-00931-z RESEARCH ARTICLE Open Access An updated tribal classification of Lamiaceae based on plastome phylogenomics Fei Zhao1†, Ya-Ping Chen1†, Yasaman Salmaki2, Bryan T. Drew3, Trevor C. Wilson4, Anne-Cathrine Scheen5, Ferhat Celep6,7, Christian Bräuchler8, Mika Bendiksby9,10, Qiang Wang11, Dao-Zhang Min12, Hua Peng1, Richard G. Olmstead13,BoLi12* and Chun-Lei Xiang1* Abstract Background: A robust molecular phylogeny is fundamental for developing a stable classification and providing a solid framework to understand patterns of diversification, historical biogeography, and character evolution. As the sixth largest angiosperm family, Lamiaceae, or the mint family, consitutes a major source of aromatic oil, wood, ornamentals, and culinary and medicinal herbs, making it an exceptionally important group ecologically, ethnobotanically, and floristically. The lack of a reliable phylogenetic framework for this family has thus far hindered broad-scale biogeographic studies and our comprehension of diversification. Although significant progress has been made towards clarifying Lamiaceae relationships during the past three decades, the resolution of a phylogenetic backbone at the tribal level has remained one of the greatest challenges due to limited availability of genetic data. Results: We performed phylogenetic analyses of Lamiaceae to infer relationships at the tribal level using 79 protein-coding plastid genes from 175 accessions representing 170 taxa, 79 genera, and all 12 subfamilies. Both maximum likelihood and Bayesian analyses yielded a more robust phylogenetic hypothesis relative to previous studies and supported the monophyly of all 12 subfamilies, and a classification for 22 tribes, three of which are newly recognized in this study. As a consequence, we propose an updated phylogenetically informed tribal classification for Lamiaceae that is supplemented with a detailed summary of taxonomic history, generic and species diversity, morphology, synapomorphies, and distribution for each subfamily and tribe. Conclusions: Increased taxon sampling conjoined with phylogenetic analyses based on plastome sequences has provided robust support at both deep and shallow nodes and offers new insights into the phylogenetic relationships among tribes and subfamilies of Lamiaceae. This robust phylogenetic backbone of Lamiaceae will serve as a framework for future studies on mint classification, biogeography, character evolution, and diversification. Keywords: Lamiaceae, Lamioideae, Mints, Phylogenomics, Tribal relationships * Correspondence: [email protected]; [email protected] †Fei Zhao and Ya-Ping Chen contributed equally to this work. 12Research Centre of Ecological Sciences, College of Agronomy, Jiangxi Agricultural University, Nanchang 330045, China 1CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Zhao et al. BMC Biology (2021) 19:2 Page 2 of 27 Background gynoecial structure. Although a deeply four-lobed ovary Lamiaceae, generally known as the mint family, have with a gynobasic style is typical for most traditionally long been known for their aromatic oils, which have recognized Lamiaceae (i.e. Lamiaceae s.s.), and an played an undeniably significant role within culinary, unlobed ovary with a terminal style is typical of most medicinal, and horticultural aspects of human history. Verbenaceae, there exists in both families a continuum Species of Lamiaceae are of wide economic importance in extent of lobing and separation of fruits into single as sources of wood (e.g., Tectona grandis L. f.), landscape seeded units [9]. Noting this, Cantino [9, 10] carried out ornamentals (e.g., scarlet sage [Salvia splendens Sellow a cladistic analysis of the Lamiaceae s.s. and the Verbe- ex Wied-Neuw.]), cosmetics (e.g., lavender [Lavandula naceae s.l. based on 85 morphological and anatomical angustifolia Mill.]), culinary herbs (e.g., basil [Ocimum characters, which provided support to reject that the basilicum L.], oregano [Origanum vulgare L.], thyme Lamiaceae s.s. was monophyletic, demonstrating several [Thymus vulgaris L.]), and medicinal herbs (e.g., Korean clades of the Verbenaceae s.l. recovered among clades of mint [Agastache rugosa (Fisch. & C.A. Mey.) Kuntze], the Lamiaceae s.s. Based on these results, Cantino et al. peppermint [Mentha × piperita L.]). Despite the recogni- [11] published a list of subfamilies and genera of the tion of this family (Lamiaceae s.s.) from advances in sys- Lamiaceae s.l. that had been proposed earlier by Junell tematics and taxonomy of the late twentieth century, the [12]. This incorporated the transfer of the cymose sub- family has historically been considered a “natural” group families Caryopteridoideae, Chloanthoideae, Viticoideae, based on a combination of readily recognizable features Symphorematoideae, and tribe Monochileae to the ex- such as an herbaceous habit, quadrangular stems, oppos- panded Lamiaceae, rendering the Verbenaceae s.s. as ite phyllotaxy, bilabiate flowers, a gynobasic style, and only the subfamily Verbenoideae. Verbenaceae s.s. can four nutlets. However, morphological and molecular be recognized by having racemose inflorescences, tricol- phylogenetic studies in the past three decades have sig- porate pollen, and ovules attached to the carpel margins, nificantly changed the concept of the family, and an ex- while the Lamiaceae s.l. generally possess thyrsoid inflo- panded Lamiaceae (Lamiaceae s.l.) is now widely rescences, colpate pollen, and ovules attached to the accepted. As currently circumscribed, Lamiaceae com- sides of the false septa of ovary [13]. Moreover, the Ver- prise more than 230 genera and over 7000 species, mak- benaceae s.s. have thickened stigma lobes with conspicu- ing it the sixth largest angiosperm family and the largest ous stigmatic tissue, hypocrateriform corollas with family in the order Lamiales [1–3]. Although unequivo- included stamens, and usually terete stems, whereas in cally shown to be members of the family, inclusion of the Lamiaceae s.l., stigma lobes are slender with incon- some disparate groups such as Vitex L. (originally placed spicuous stigmatic tissue, corollas that are rarely hypo- in Verbenaceae because they were trees with fleshy crateriform, and stems are typically quadrangular. Since fruits) has challenged the earlier concepts of the family. Cantino et al. [11], the expanded concept of the Lamiaceae Early infrafamilial classifications within Lamiaceae s.l. has been consistently supported as monophyletic by were predominately based on the treatment of Bentham molecular phylogenetic studies [14–20] and is widely ac- [4], who divided the family into eight tribes. Briquet [5], cepted in various classifications [1, 3]. We acknowledge for example, followed the division of Bentham [4], but these results and use the names Lamiaceae and Verbena- raised some of the tribes to subfamilial rank and merged ceae in their contemporary circumscription. Though today four tribes into the single large subfamily Lamioideae. both Lamiaceae and Verbenaceae are placed within “core Erdtman [6], however, recognized only two subfamilies Lamiales” of the asterids, they have unexpectedly not been based on palynological distinctions, viz., Lamioideae recovered as sister taxa despite their morphological simi- (with tricolpate pollen shed at the two-celled stage) and larities: Lamiaceae belong to a clade that includes Maza- Nepetoideae (with hexacolpate pollen shed at the three- ceae, Phrymaceae, Wightiaceae, Paulowniaceae, and celled stage). Combining the classifications of Briquet [5] Orobanchaceae, whereas Verbenaceae are recovered as and Erdtman [6], Wunderlich [7] recognized six subfam- sister to Thomandersiaceae [18, 21, 22]. ilies within Lamiaceae, rejecting Lamioideae as circum- Following Cantino et al. [11], Harley et al. [1]published scribed by Briquet [5] and accepting a subfamily a global, genus-level taxonomic conspectus of Lamiaceae. Nepetoideae close to that of Erdtman [6]. Cantino and Except for the ten genera Acrymia Prain, Callicarpa L., Sanders [8] revealed that Nepetoideae sensu Erdtman [6] Cymaria Benth., Garrettia H.R. Fletch., Holocheila (Kudô) is monophyletic with several synapomorphies, whereas S. Chow, Hymenopyramis Wall. ex Griff.,